314 SHORT COMMUNICATION Cruz et al.

Prevalence of larvae of the bot simulans (Diptera, Oestridae) on Gracilinanus microtarsus (Didelphimorphia, Didelphidae) in southeastern Cerrado from Brazil

Leonardo Dominici Cruz1, Fernanda Rodrigues Fernandes2 & Arício Xavier Linhares3

1Programa de Pós-Graduação em Ciências Biológicas (Zoologia), Caixa Postal 199, Instituto de Biociências, Universidade Estadual Paulista Júlio de Mesquita Filho, Avenida 24-A, 1515, 13506-900 Rio Claro-SP, Brasil. [email protected] 2Programa de Pós-Graduação em Ecologia, Caixa Postal 6109, Instituto de Biologia, Universidade Estadual de Campinas, 13083-970 Campinas- SP, Brasil. [email protected] 3Departamento de Parasitologia, Caixa Postal 6109, Instituto de Biologia, Universidade Estadual de Campinas, 13083-970 Campinas-SP, Brasil. [email protected]

ABSTRACT. Prevalence of larvae of the bot fly Cuterebra simulans (Diptera, Oestridae) on Gracilinanus microtarsus (Didelphimorphia, Didelphidae) in southeastern Cerrado from Brazil. The prevalence of Cuterebra simulans bot fly on marsupial Gracilinanus microtarsus was compared between sexes and seasons of the year. No significant difference was observed between females and males but prevalence was higher in warm-wet season than cool-dry season. This pattern agree with observations of others studies with oestrids in southern Neotropical areas, suggesting the occurrence of latitudinal change in the peak of bot flies reproductive activity related to seasons of the year along these systems. This is the first record of C. simulans larvae parasitism on G. microtarsus and its occurrence in southern areas of the Neotropical region.

KEYWORDS. Bot fly; ; opossum; parasitism.

RESUMO. Prevalência de parasitismo de de Cuterebra simulans (Diptera, Oestridae) em Gracilinanus microtarsus (Didelphimorphia, Didelphidae) no Cerrado do sudeste do Brasil. A prevalência de parasitismo das larvas da mosca Cuterebra simulans no marsupial Gracilinanus microtarsus foi comparada entre os sexos e estações do ano. Machos e fêmeas não apresentaram diferenças significativas, mas a prevalência de parasitismo foi mais elevada na estação quente- úmida que na estação fria-seca. Este padrão está de acordo com as observações de outros estudos com moscas da família Oestridae realizados nas áreas ao sul da região Neotropical, sugerindo a ocorrência de mudanças latitudinais nos picos de atividades reprodutivas destas moscas em relação às estações do ano ao longo destes sistemas. Este também é o primeiro registro da ocorrência de C. simulans em áreas mais ao sul da região Neotropical e do parasitismo de suas larvas em G. microtarsus.

PALAVRAS-CHAVE. Miíase; marsupial; parasitismo; mosca do berne.

Bot flies of the genus Cuterebra are restricted to the New demonstrate that such flies may be multivoltine (Bergallo et World and are distributed throughout most of the temperate al. 2000; Adler et al. 2003). and tropical areas. Their larvae are obligatory parasites of Marsupials are also natural hosts of bot fly larvae and are , producing myiasis in dermic and subdermic tissues distributed widely in New World tropics with most species of these (Catts 1982; Pape 2001). There is almost 70 found in South America, principally represented by species of Cuterebra and these flies are one of the most highly Didelphimorphia order, or opossums, with approximately 93 studied groups of parasites of New World wild mammals species (Eisenberg & Redford 1999). Nevertheless, there are (Slansky 2007). However, the knowledge available on the only a few studies and anecdotal records on the prevalence ecology and natural history of most species comes from and dynamics of bot fly larval parasitism in marsupials (Fonseca studies carried out in temperate regions (e.g. Wolf & Batzli 1941; Guimarães 1971; Bossi & Bergallo 1992; Pujol-Luz et al. 2001; Alcock & Kemp 2004; Jaffe et al. 2005). In the Neotropical 2004). The gracile mouse opossum Gracilinanus microtarsus region, the studies concerning the prevalence and dynamics (Wagner, 1842) is a small (20-45 g), solitary, arboreal, nocturnal, of bot fly larval parasitism in wild mammals are scarce and and insectivorous marsupial commonly found in the Atlantic have been carried out mainly with . These studies have rainforest and forested physiognomies interspersed in showed higher prevalence of bot fly larval parasitism in warm- savannas in the Cerrado biome. This species shows sexual wet season of the year, although few longitudinal studies size dimorphism with adult males being larger than adult

Revista Brasileira de Entomologia 53(2): 314–317, junho 2009 Prevalence of larvae of the bot fly Cuterebra simulans (Diptera, Oestridae) on Gracilinanus microtarsus 315 females, and has a markedly seasonal pattern of reproduction occurring in the warm-wet season when males competing for access to females (Costa et al. 2003; Martins et al. 2006). Males and females may differ in prevalence of parasites due to fundamental biological differences between sexes. For example, in reproduction period males may be engaged in sexual competition for mating opportunities, which is under control of hormones that negatively affect the immune system and increase the vulnerability to parasites (Møller et al. 1999). On the other hand, females may increase their home range areas to found more food due to increase energetic requirements associated with pregnancy and lactation that may increase their probabilities of being infested for parasites (Krasnov et al. 2005) or they may restricted their activity areas near to nests that may increase the chance of the mobile parasites found them. Since the studies in the Neotropical have showed high seasonality in the prevalence of parasitism by Cuterebra larvae and that biological differences between hosts sexes may affect parasitism, the aim of our study was to investigate the differential prevalence of the bot flies larvae parasitism between sexes and seasons of the year on G. microtarsus. This study was carried out at the Reserva Biológica de Mogi Guaçu (22º 15’/22º 18’S, 47º 08’/47º 13’W), located in the city of Mogi Guaçu, São Paulo state, southeastern Brazil. Vegetation consists of Cerrado, which is a tropical savannah formation comprising different vegetation physiognomies that differ in the density and composition of plants of the woody layer and the ground layer, forming a continuum from open Fig. 1. Map of Cuterebra simulans distribution in South America. Grey and dry grassland to dense forest (Oliveira-Filho & Ratter areas represent well-known distributions (Peru; A – Paramaribo, 2002; Silva & Bates 2002). The climate of the region has two Suriname; B – Belém, Brazil) according to Guimarães & Papavero well-defined seasons: a warm-wet season from October to (1999). Black area represents the new record of occurrence (C – Mogi March when the temperature varies of 16.8°C to 36.7°C and Guaçu, Brazil). mean rainfall is 187.7 mm, and a cool-dry season from April to September when the temperature varies of 5.2°C to 31.3°C and mean rainfall is 46.2 mm. parasitism in females was 0.32 and 0.28 in males but the The individuals of the G. microtarsus were trapped monthly difference between sexes was not significant (Z = 0.395; p = from September 2005 to August 2006, over 10 consecutive 0.348). The number of the bot flies larvae in each host varied nights each month and marked with a numbered ear tag and of 1 to 5. Some individuals showed repeated infestations by their sex was recorded. We set an 11 x 11 trapping grid with 121 larvae of the C. simulans in different months of the same trapping-stations located 15 m from each other. We visually season and in different season after the emergence of the bot examined all the individuals to record the occurrence or flies larvae previously recorded, but these events were absence of the bot flies larvae parasitism and the number of considered as independent events to estimation of the the larvae in each host. Some parasitized individuals were kept prevalence in each season. Thus, the prevalence in each season at the laboratory to allow natural emergence of the bot flies was estimated by the number of times that one individual larvae. After emergence the pupae were maintained buried in became infested for parasites. In all study, ninety-four events moist sand in gauzed-covered glass cups at ambient of G. microtarsus examination (62 in warm-wet season and 32 temperature until adult flies emerged (pupariation lasted 30 to in cool-dry season) occurred. The prevalence of bot flies larvae 32 days). Three adult bot flies emerged and they were identified parasitism in warm-wet season was 0.34 and 0.06 in cool-dry as Cuterebra simulans (Austen, 1933). The prevalence of bot season and the difference between season was significant (Z flies larvae parasitism of the C. simulans was calculated in = 2.952; p = 0.0016). agreement to Bush et al. (1997) and the prevalence between Some studies carried out in Neotropical systems have sex and seasons were compared with binomial test for unequal showed a sex-biased larvae parasitism of the oestrids bot flies proportions at the level 0.05 of the significance (Zar 1998). in rodents with males more infested than females (Bergallo et We captured 78 individuals of the G. microtarsus (38 al. 2000; Manrique-Saide et al. 2000), females more infested females and 40 males). The prevalence of bot flies larvae than males (Brigada et al. 1992) or no sex-biased bot flies larvae

Revista Brasileira de Entomologia 53(2): 314–317, junho 2009 316 Cruz et al. infestation (Adler et al. 2003) and these patterns always are Acknowledgements. We thank João Del Giudice Neto and Marcos discussed in terms of the biological sexual differences of the Mecca Pinto for the authorization to carry out the research at the Reserva Biológica de Mogi Guaçu, Sérgio F. Reis for logistical support, hosts. Our results did not show differences in the parasitism FAPESP and CNPq for financial support. prevalence of the C. simulans larvae between males and females of the G. microtarsus, although males and females showed differences in movement patterns in study area where males REFERENCES showed larger home ranges than females (Fernandes 2007) and distinct signals of the high level stress in the reproduction Adler, G. H.; S. L. Davis & A. Carvajal. 2003. 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Received 30/10/2008; accepted 17/03/2009

Revista Brasileira de Entomologia 53(2): 314–317, junho 2009